Range-Wide Latitudinal and Elevational Temperature

Range-Wide Latitudinal and Elevational TemperatureGradients for the World’s Terrestrial Birds: Implicationsunder Global Climate ChangeFrank A. La Sorte1*, Stuart H. M. Butchart2, Walter Jetz3, Katrin Bohning-Gaese4,5

1 Cornell Laboratory of Ornithology, Cornell University, Ithaca, New York, United States of America, 2 BirdLife International, Cambridge, United Kingdom, 3 Department of

Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States of America, 4 Biodiversity and Climate Research Centre (BiK-F), Senckenberg

Gesellschaft fur Naturforschung, Frankfurt (Main), Germany, 5 Department of Biological Sciences, Goethe Universitat, Frankfurt (Main), Germany

Abstract

Species’ geographical distributions are tracking latitudinal and elevational surface temperature gradients under globalclimate change. To evaluate the opportunities to track these gradients across space, we provide a first baseline assessmentof the steepness of these gradients for the world’s terrestrial birds. Within the breeding ranges of 9,014 bird species, wecharacterized the spatial gradients in temperature along latitude and elevation for all and a subset of bird species,respectively. We summarized these temperature gradients globally for threatened and non-threatened species anddetermined how their steepness varied based on species’ geography (range size, shape, and orientation) and projectedchanges in temperature under climate change. Elevational temperature gradients were steepest for species in Africa,western North and South America, and central Asia and shallowest in Australasia, insular IndoMalaya, and the Neotropicallowlands. Latitudinal temperature gradients were steepest for extratropical species, especially in the Northern Hemisphere.Threatened species had shallower elevational gradients whereas latitudinal gradients differed little between threatened andnon-threatened species. The strength of elevational gradients was positively correlated with projected changes intemperature. For latitudinal gradients, this relationship only held for extratropical species. The strength of latitudinalgradients was better predicted by species’ geography, but primarily for extratropical species. Our findings suggestthreatened species are associated with shallower elevational temperature gradients, whereas steep latitudinal gradients aremost prevalent outside the tropics where fewer bird species occur year-round. Future modeling and mitigation effortswould benefit from the development of finer grain distributional data to ascertain how these gradients are structuredwithin species’ ranges, how and why these gradients vary among species, and the capacity of species to utilize thesegradients under climate change.

Citation: La Sorte FA, Butchart SHM, Jetz W, Bohning-Gaese K (2014) Range-Wide Latitudinal and Elevational Temperature Gradients for the World’s TerrestrialBirds: Implications under Global Climate Change. PLoS ONE 9(5): e98361. doi:10.1371/journal.pone.0098361

Editor: David L. Roberts, University of Kent, United Kingdom

Received February 17, 2014; Accepted May 1, 2014; Published May 22, 2014

Copyright: � 2014 La Sorte et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This work was funded through a postdoctoral fellowship at the Cornell Lab of Ornithology. The funders had no role in study design, data collection andanalysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

* E-mail: [email protected]

Introduction

A variety of responses are available for species as global climate

change progresses [1,2] and changing climatic conditions increas-

ingly impact species’ performance and fitness. The two primary

options, which are not necessarily independent, are for species’

populations to shift their geographic ranges to regions containing

suitable climatic conditions, or to remain and adapt phenotypically

or genetically [3,4]. One of the most important immediate

responses is for species to track their geographic climatic

associations across space. This may be possible provided that

opportunities are available for geographic range-shifts, species

have the physiological and behavioral capacity to take advantage

of them, and they can keep pace with the velocity of climate

change [5]. Geographic niche tracking has been observed under

climate change over geological time scales [6] and more recently

under modern climate change [7,8].

Two environmental gradients appear particularly relevant when

considering geographic niche tracking under past and current

climate change: surface latitudinal and elevational temperature

gradients. Both gradients represent natural environmental features

whose location and general form remain consistent across

ecological time-scales, and there is empirical evidence that many

taxa including birds are currently tracking these gradients under

climate change [7,9]. Latitudinal temperature gradients are

strongest outside the tropics, especially in the Northern Hemi-

sphere where the most extensive land masses are located [10].

Elevational temperature gradients are stronger and less variable

than latitudinal temperature gradients but are geographically

more restricted [11]. Latitudinal and elevational temperature

gradients are not equally available for all species nor are they

uniformly distributed within species’ geographic ranges. Under

current climate change projections, there is no evidence to suggest

the strength of elevational temperature gradients are expected to

change; whereas there is evidence that the strength of latitudinal

temperatures gradients may change over broad geographic regions

[2]. Due to latitudinal asymmetry in surface warming, latitudinal

temperature gradients are projected to weaken in the Northern

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Hemisphere [2,12], which is expected to result in diminished

seasonality and increased vegetation growth at the high northern

latitudes [13,14].

Life history, morphological, and physiological traits are known

to vary among species’ populations at geographic scales [15] and,

in some cases, this variation is correlated with latitudinal or

elevational gradients [16,17] and associated temperature gradients

[18]. This variation in ecological traits across latitudinal or

elevational gradients can in turn affect reproductive potential and

rates of population growth, especially at range limits [19,20].

Under climate change, the structure of latitudinal and elevational

temperature gradients can be modified, affecting population

growth rates, especially at the leading and trailing edge of the

gradient within species’ ranges [21,22]. Specifically, climate

change can result in population growth increasing at the leading

edge and declining at the trailing edge of the gradient, with the

increased likelihood of range shifts at the leading edge and

extirpation of populations at the trailing edge.

The strength of latitudinal and elevational temperature

gradients within species current geographic ranges relative to

projected changes in temperature under climate change can

determine the potential for range-shifts to occur under climate

change. For species whose geographic ranges have similar spatial

dimensions in relationship to latitudinal or elevational temperature

gradients, the steeper the gradient, the broader the species’

geographic climatic niche (i.e., species’ association with climatic

conditions across space) and the greater the likelihood that a larger

component of current climatic associations will be retained within

the geographic range as temperatures increase (Figure 1A,B,C). In

contrast, the shallower the gradient, the narrower the species’

geographic climatic niche and the smaller the likelihood that a

significant geographic component of current climatic conditions

will be retained within the geographic range as temperatures

increase (Figure 1D,E,F). One potential consequence of shallow

latitudinal or elevational temperature gradients is the formation of

range-shift gaps [10]. Here, increasing temperatures can result in

the complete loss of current climatic associations within species’

current geographic ranges, an outcome that may substantially

hinder successful range-shifts. Range-shift gap width is also likely

to be negatively correlated with the strength of the temperature

gradients (Figure 1), suggesting species’ distributions containing

very weak gradients, as found with many tropical species, are

particularly susceptible to the consequences of climate change

[10]. In total, climate change can modify latitudinal or elevational

temperature gradients within species’ geographic ranges, which in

turn can alter population dynamics at range boundaries and

range-shift potential based on the strength of those gradients

relative to the magnitude of climate change.

Here, we estimate latitudinal and elevational temperature

gradients within the geographic ranges of ca. 90% of the world’s

avifauna, numbering 9,014 species. To evaluate whether bird

species that are currently threatened with extinction also face

particularly high risks under climate change, we structure our

analysis to compare species classified as threatened (n = 878) vs.

non-threatened with extinction (n = 8,136) on the IUCN Red List

[23]. We additionally examine the ability of species’ geography

(range size, shape, and orientation relative to the equator) to

explain variation in elevational and latitudinal temperature

gradients among species. These characteristics of species’ ranges

tend to be geographically similar across taxa [24] and are

determined in part by spatial variation in climate and topography

[25]. Lastly, to assess the degree of correspondence between

projected warming and the availability of elevational and

latitudinal temperature gradients within species’ ranges, we

consider how gradient strength is related to variation in projected

changes in temperature under climate change.

Materials and Methods

Data sources and preparationWe acquired range maps for the world’s birds from BirdLife

International and NatureServe [26] whose data sources are

described in Buchanan, Donald and Butchart [27]. We considered

breeding/resident ranges only and excluded species that were not

well suited for our analysis, specifically those associated with

marine environments. This resulted in a total of 9,014 extant

species for analysis (see Table S1). These species were classified as

either threatened (n = 878) or non-threatened with extinction

(n = 8,136) using the IUCN Red List [23]. Here threatened refers

to species identified as vulnerable, endangered, or critically

endangered under the IUCN Red List.

Species range data was analyzed using a gridded system having

a cylindrical equal-area projection and a cell area of 3,091 km2.

We defined species’ geographic breeding ranges as the spatial

combination of equal area cells with $50% terrestrial surface area

(based on the proportion of the cell that contained non-marine

terrain) that intersected each species’ geographic range polygon.

We placed each species into one of six biogeographical realms [28]

based on the realm that contained the greatest proportion of each

species’ gridded range (Nearctic, Palaearctic, IndoMalaya, Neo-

tropics, Afrotropics, and Australasia). Species whose ranges

occurred primarily in Antarctica or Oceania were excluded from

analysis. From the 9,014 species, we acquired minimum and

Figure 1. Conceptual figures of six geographic range-shiftscenarios for species containing steep (A,B,C) or shallow(D,E,F) latitudinal or elevational temperature gradients withintheir geographic ranges. The spatial breadth of the latitudinal orelevational gradient within the geographic range is identical in eachcase. The current temperature gradient (solid line) and the projectedtemperature gradient under climate change (dashed line) are shown foreach scenario. The location of the geographic range of the speciesalong the temperature gradient is depicted with a bold line betweenthe solid blue and red arrows. The species’ leading (blue arrow) andtrailing (red arrow) range limits are shown based on the currentgradient (solid arrows) and the projected gradient under climatechange (dashed arrows). Three gradations in projected climate changeare shown: weak (A, D), moderate (B, E), and strong climate change (C,F). The horizontal dotted lines identify the boundaries of each species’geographic climatic niche as defined along the temperature gradient.Everything else being equal, species with steeper environmentaltemperature gradients have broader geographic climatic niches andneed to shift their geographic range less in order to track climatechange.doi:10.1371/journal.pone.0098361.g001

Temperature Gradients for the World’s Terrestrial Birds


maximum elevation associations for 4,978 species from BirdLife

International [23]. The distribution of these species across the six

realms did not show geographic biases, with the proportion of

species in each realm not diverging significantly from expectation

(x2 = 0.029, df = 5, P = 1.0).

Temperatures within species’ geographic ranges were estimated

using the annual average of 1950–2000 average-monthly temper-

atures from WorldClim [29] gridded and analyzed at a 30-arcsec

resolution (ca. 1 km at the equator). Elevations within species’

ranges were estimated using the USGS global digital elevation

model (GTOPO30) gridded and analyzed at a 30-arcsec

resolution. Tropospheric lapse rates, the association between

temperature and elevation within the troposphere, were estimated

globally using a gridded model at a resolution of 2.5u (ca. 278 km

at the equator) for the period 1948–2001 [11].

Broad-scale, expert-based range maps are only coarsely defined

estimates of species occurrence and reliably characterize presences

only above 100 km grain [30,31]. Here, we are interested in the

form of latitudinal and elevational temperature gradients (i.e.,

shallow or steep) as defined across the geographic breadth of

species’ distributions independent of patterns of occurrence. The

use of relatively high resolution global estimates of temperature

and elevation provided the detail of data necessary to estimate the

full structure of these gradients for individual species, especially in

situations where geographic ranges were small or temperature

gradients were non-linear. For the purpose of this baseline study

we assume that low probability of occurrence naturally incurred at

the finer spatial grain are not biasing the geographic and species

comparisons. We acknowledge that this assumption is not

necessarily valid and will require careful follow-up assessments at

local scales or at broader scales once more detailed distribution

data becomes available.

Projected changes in temperature (temperature anomalies) were

estimated using projections averaged over four Atmosphere Ocean

General Circulation Models (AOGCMs). The four AOGCMs

were CNRMCM3, CSIRO-Mk3.0, ECHam5, and MIROC 3.2.

The gridded projections from these models were downscaled to 30

arc-minute resolution using pattern scaling with the MarkSim

weather generator [32]. The projections were based on the A2

scenario, which is currently considered to be the most relevant

under current greenhouse gas emission rates [33,34]. The

anomalies represent the change in temperature between the

twentieth century control 30-year normal (1961–1990) and the 30-

year period 2081–2100. The temperature anomalies were

bilinearly interpolated to match the resolution of the 3,091 km2

equal-area grid.

Elevational temperature gradientsWe estimated latitudinal and elevational temperature gradients

separately in order to better represent each gradient’s unique

characteristics. The presence of elevational temperature gradients

is dictated by the presence of mountain systems or orographic

features, which show substantial geographic variation (see Figure

S1). Mountain systems often contain strong topographic hetero-

geneity resulting in a mosaic of climatic conditions, which are

poorly estimated using interpolated weather station data [35,36].

Here, we use elevation data, which does not rely on similar

interpolation methods, to estimate elevational temperature gradi-

ents within species’ ranges.

Unlike latitudinal temperature gradients, the strength of

elevational temperature gradients are broadly consistent from

the equator to the poles. Tropospheric lapse-rate averages 6.2uCkm21 over the continents, with a range of 4.5 to 6.5uC km21 from

the polar latitudes to the equator, respectively [11]. To account for

this geographic variation, we calculated the average tropospheric

lapse-rate within each species’ geographic range. To account for

the high variability in the extent and spatial distribution of

orographic features and the decline in terrestrial area with

increasing elevation resulting in strongly skewed distributions of

elevation within species’ ranges, we estimated two components of

the elevational temperature gradient for each species: (1) the

overall magnitude and (2) the evenness of the gradient. We then

combined tropospheric lapse-rate with magnitude and evenness to

generate one metric designed to represent the overall strength of

elevational temperature gradients within each species’ range.

More specifically, for species whose minimum and maximum

elevation associations had both been estimated (n = 4,978), we

excluded elevations within the geographic range below and above

these associations. We then identified the actual minimum and

maximum elevations within each species’ range based on our

gridded elevation data, which in combination with species’

documented elevation associations were used to calculate each

species’ realized vertical range extent. Vertical range extent was

used to estimate the magnitude of each species’ elevational

temperature gradient. To assess how evenly the vertical range

extent was distributed across each species’ range, we first summed

the number of 30 arc-second elevation cells in all 100-m

elevational bands found within each species range. We then used

the Lorenz curve and associated Gini coefficient [37–39],

explained below, to estimate how evenly the cells were distributed

across elevation bands. Here, the 100-m bands were first ranked

from lowest to highest elevation. The frequency of cells within

these bands was then used to plot the Lorenz curve, i.e. the

cumulative proportion of the number of cells in each band (x-axis)

against the corresponding cumulative proportion of their eleva-

tions (y-axis). Gini coefficients (or Gini ratio) were then calculated,

which is defined as twice the area contained between the Lorenz

curve and the line of perfect equality (or perfect evenness). The

Gini coefficient has a range from 0 to 1, high to low evenness,

respectively. To ease interpretation, for each species we took the

product of the vertical range extent, average tropospheric lapse

rate, and the inverse of evenness (1 – Gini coefficient) to generate a

single index for the elevational temperature gradient. We interpret

this index as the overall strength of the elevational temperature

gradient across each species’ range: larger values indicate the

presence of a strong and more evenly distributed gradient; lower

values indicate the presence of a weak gradient due to either a

small vertical range extent or an unevenly distributed vertical

range extent.

Latitudinal temperature gradientsOutside the tropics, average annual temperature declines on

average 0.7uC for each degree of latitude in the Northern

Hemisphere and on average 0.5uC for each degree of latitude in

the Southern Hemisphere (Figure S2). With one degree of latitude

equal to approximately 111 km, this translates to a decline of 1uCfor every 150 km in the Northern Hemisphere and a decline of

1uC for every 197 km in the Southern Hemisphere.

We estimated the latitudinal temperature gradient within the

breeding ranges of 9,014 species while controlling for variation in

elevation. For our approach, we first found the average

tropospheric lapse rate within each species’ range. We then

compiled gridded 30 arc-second average annual temperatures and

elevations within each species’ range. We chose annual average

temperature because matching each species’ breeding season

distribution with their unique breeding season temperatures,

especially for migratory species that only spend a few weeks to

months on the breeding grounds, was not feasible. A likely



consequence of using annual average temperature is that estimates

of latitudinal temperature gradients for species that breed outside

the tropics are likely to be steeper than they would be if estimates

were based on the breeding season alone. Beyond these qualitative

differences, using annual average temperature is unlikely to alter

our qualitative conclusions. To control for the effect of elevation

on temperature, we applied quantile regression to temperature as

a function of elevation for 11 quantiles (0.0, 0.1,…0.9, 1.0). The

residuals for the quantile whose slope most closely matched the

tropospheric lapse rate estimated for each species was retained for

further analysis. This approach allowed us to interpret latitudinal

temperature gradients as the gradient along a fixed elevation

within each species’ range.

The relationship between these residuals and latitude was then

assessed for each species using segmented linear regression [40]. If

species’ ranges occurred in both hemispheres, the range was first

split in half at the equator and each portion was analyzed

separately. We tested if the relationship between temperature and

latitude contained one or two segments using Davie’s test [41],

which tests for a non-zero difference in the slope parameters of the

segmented relationship. Relationships with two segments are more

likely to occur if species’ distributions are intersected by the

Tropics of Cancer or Capricorn (Figure S2). When there was

statistical evidence for a segmented relationship, we estimated a

break point between segments and slope coefficients for each

segment. When there was no statistical evidence for multiple

segments, a single slope coefficient was estimated. Coefficients

estimated south of the equator were multiplied by 21 to allow for

comparison between the two hemispheres (i.e., latitudinal

temperature gradients north and south of the equator are both

negative; Figure S2). For species whose ranges were estimated by

one slope coefficient, this coefficient was used to represent the

overall gradient. For species whose ranges contained multiple

slope coefficients, we used a weighted average to summarize the

gradient. Weights were based on the latitudinal extent of the

region where each slope coefficient was estimated. Based on this

procedure, larger negative values indicate steeper latitudinal

temperature gradients and values approaching zero indicate

shallower latitudinal temperature gradients.

AnalysisTo summarize how steep elevational and latitudinal tempera-

ture gradients are on average within species’ ranges globally, we

first calculated the average elevational temperature gradient and

median latitudinal temperature gradient within each equal-area

cell for all species whose geographic ranges intersected that cell.

To summarize how gradients differed for threatened and non-

threatened species, we quantified how the gradients varied by

species’ median latitude. This analysis was implemented separately

for species in each of the six biogeographical realms. For

elevational temperature gradients, we used generalized additive

models (GAM; [42]) with a Gaussian error distribution. For

latitudinal temperature gradients, we used robust MM-type

polynomial regression [43,44]. GAM was selected because it

adjusts automatically to the nonlinear associations observed

between elevational temperature gradients and species’ median

latitude. This feature also supported the use of GAM to examine

how species richness, range size, elevational extent, and Gini

coefficient varied by species’ median latitude for threatened and

non-threatened species. Robust polynomial regression was selected

for latitudinal temperature gradients because of the presence of

many extreme outliers that were poorly modeled with GAM. In

addition, the general curvilinear form of the relationship was well

represented with a polynomial function. The order of the

polynomial function was determined using robust Wald-type or

deviance-type tests of nested model pairs. Median latitude was

defined as the median of the full latitudinal extent of each species’

range.

We used robust multiple regression to examine the ability of

geographic and climatic predictors to explain the variability

observed in species latitudinal and elevational temperature

gradients. The four predictors were estimated within each species’

geographic range and included average projected temperature

anomaly, and geographic range size, shape, and orientation.

Range size was log10 transformed before analysis. Range shape

and orientation were estimated based on a principle component

analysis (PCA) of the latitude and longitude of the grid cells

contained within each species geographic range. PCA was

conducted using a singular value decomposition of the centered

data matrix. The square roots of the two eigenvalues were used to

estimate range shape, where the minimum eigenvalue was divided

by the maximum eigenvalue. Here, values approaching zero

indicating elongated ranges and values approaching one indicating

circular ranges. Range orientation was estimated based on the

angle of the major axis of the PCA eigenvector from the equator.

Values for range orientation were defined from 0u (parallel with

the equator) to 90u (perpendicular to the equator). We evaluated

our four predictors for multi-collinearity and singularity using

variance inflation factors (VIFs) where predictors with VIF.5

indicate cause for concern and VIF.10 indicate the presence of

significant collinearity [45]. We retained all four predictors after

they were deemed to be statistically independent (VIF#1.6).

To evaluate differences between threatened and non-threatened

species, we included in addition to the four continuous predictors,

a species’ IUCN Red List status as threatened or non-threatened

with extinction. For the analysis of the latitudinal temperature

gradient, we also considered if the median latitude of a species’

range was located within or outside the tropics. Median latitudes

between 23.5uS and 23.5uN latitude were considered tropical. The

tropical/extratropical classification was included because it

defined a major feature of the gradient (Figure S2). In total, we

examined eight robust multiple regression models that consisted of

the two gradients, the four continuous predictors, associated

categorical predictors, and all pairwise interactions.

All analyses were conducted in R version 3.0.1 [46]. Segmented

regression was conducted using the ‘segmented’ library, robust

regression using the ‘robust’ and ‘robustbase’ libraries, and GAM

using the ‘mgcv’ library [42]. We used the default optimization

procedure to estimate the degree of smoothing in the GAMs [42].

The Lorenz curves were estimated using the ‘ineq’ library and the

Gini coefficients were estimated using the ‘reldist’ library.

Results

Threatened and non-threatened bird species presented similar

latitudinal trends in species richness with peaks for both groups

occurring in the tropics (Figure 2A and Figure S3). Range sizes for

threatened species were significantly smaller on average except for

species located at the most extreme northern and southern

latitudes (Figure 2B and Figure S3). For the 4,978 species with

documented elevational associations, threatened species had

smaller vertical range extents within their geographic ranges

(Figure 2C and Figure S3) and threatened species had higher

elevational evenness within their geographic ranges in the central

tropics and more equivalent elevational evenness elsewhere

(Figure 2D and Figure S3). Projected increases in temperature

within species’ ranges were highest for species located at higher



latitudes in the Northern Hemisphere and lowest for species

located at lower latitudes in the Southern Hemisphere (Figure S4).

There was strong geographic variation in the steepness of

elevational temperature gradients (Figure 3). When considering

the combined effects of elevational extent and elevational evenness

(Figure S3) with tropospheric lapse rate, the strongest gradients

were found for species located in Africa, the western part of North

and South America, and the Tibetan Plateau region. In contrast,

species in Australasia, the islands of IndoMalaya and the lowlands

of the Neotropics had the weakest elevational temperature

gradients (Figure 3). Threatened species were associated with

weaker elevational temperature gradients across the six biogeo-

graphical realms, with the most significant differences occurring in

the Neotropics and Afrotropics (Figure 3).

After controlling for elevation, latitudinal temperature gradients

were on average shallowest for species in the tropics and steepest

for species outside the tropics (Figure 4). The steepest latitudinal

temperature gradients occurred in the Northern Hemisphere.

Australasia had the strongest gradients in the Southern Hemi-

sphere, which did not match the strength observed in the Northern

Hemisphere. There was no evidence that the latitudinal temper-

ature gradients differed between threatened and non-threatened

species across the six biogeographical realms (Figure 4).

Variation in elevational temperature gradients among species

was poorly explained by our four predictors (Table 1 and Figure

S5). Species with higher projected temperature increases and

larger geographic ranges had steeper elevational temperature

gradients, and this was the case for both threatened and non-

threatened species. Species with geographic ranges that were

elongated in shape and oriented perpendicular to the equator had

stronger gradients, and this was more pronounced for non-

threatened species.

Figure 2. Plots summarizing geographic patterns for species’ currently identified as threatened (red points; n = 878) and non-threatened (green points; n = 8,136) with extinction by the median latitude of each species’ range. (A) The number of species’ whosemedian latitudes occur within one degree latitudinal bands; (B) species’ range size; (C) the elevational extent within species’ ranges for 4,978 specieswith minimum and maximum elevation associations; and (D) the evenness of the distribution of 100 m elevations bands within species’ ranges basedon the Gini coefficient (0 = high evenness; 1 = low evenness; see Materials and Methods for details) for 4,978 species with minimum and maximumelevation associations. The trend lines are the fits of generalized additive models for species threatened (red) and non-threatened (black) withextinction.doi:10.1371/journal.pone.0098361.g002



Variation in latitudinal temperature gradients was better

explained by our four predictors, with evidence for significant

and strong differences between tropical and non-tropical species

(Table 2 and Figure S6). Tropical species had weaker relationships

for all four predictors with little evidence for differences between

threatened and non-threatened species. For threatened and non-

threatened extratropical species, species with higher projected

temperature increases, larger ranges and ranges that were

elongated in shape and oriented parallel with the equator had

steeper latitudinal temperature gradients. For threatened extra-

tropical species, gradients were even steeper for species with larger

ranges.

Discussion

Species face unique challenges under climate change, with the

availability and strength of range-shift opportunities along

latitudinal or elevational temperature gradients playing a signif-

Figure 3. The elevation temperature gradient index summarized across species’ geographic ranges (map) and summarized withinsix biogeographical realms (plots) as a function of the median latitude of each species’ range. The temperature gradient was estimatedspatially within species’ current ranges (see Materials and Methods for details). In the plots, red points are threatened species (n = 766) and greenpoints are non-threated species (n = 4,212). Trend lines are the fits of generalized additive models for threatened (red) and non-threatened species(black). The solid line is the equator and the dashed lines are the Tropics of Cancer and Capricorn (23.5uN and 23.5uS latitude, respectively).doi:10.1371/journal.pone.0098361.g003



icant role in determining species’ likelihood of persistence. In this

study we provide the first estimation of these gradients for the

world’s avifauna relative to species’ IUCN Red List category,

geography, and projected exposure to climate change. Our

approach expands upon current methods for estimating species’

geographic climatic associations by measuring these two gradients

individually using fine-grained environmental data, which more

accurately captures their unique spatial structures. The application

of this approach has the potential to increase biological realism

and predictive quality in current large-scale modeling efforts by

removing problematic assumptions and minimizing potential

biases. Our findings suggest threatened species are at a distinct

disadvantage globally based on their association with shallower

elevational temperature gradients. Latitudinal temperature gradi-

ents are primarily relevant for species located outside the tropics, a

region where few bird species occur year-round, including

threatened species whose associations with latitudinal temperature

gradients did not differ from non-threatened species. Our results

Figure 4. The latitudinal temperature gradient index summarized across species’ geographic ranges (map) and summarized withinsix biogeographical realms (plots) as a function of the median latitude of each species’ range. The temperature gradient was estimatedspatially within species’ current ranges (see Materials and Methods for details). In the plots, red points are threatened species (n = 878) and greenpoints species non-threated species (n = 8,136). Trend lines are the fits of generalized additive models for threatened (red) and non-threatenedspecies (black). The solid line is the equator and the dashed lines are the Tropics of Cancer and Capricorn (23.5uN and 23.5uS latitude, respectively).doi:10.1371/journal.pone.0098361.g004



also indicate a degree of correspondence between range-shift

opportunities and climate change, in that species in regions that

are projected to experience greater warming are more likely to be

associated with steeper temperature gradients.

The strength of latitudinal temperature gradients is determined

in part by the location, size, shape and orientation of species’

geographic ranges. Not surprisingly, the strongest latitudinal

temperature gradients were associated with species whose ranges

occurred outside the tropics, especially at the higher latitudes in

the North Hemisphere where the largest land masses are located.

Species in these regions tend to have larger geographic ranges (see

Figure 2B) and ranges that tend to be elongated parallel to the

equator. As our results indicate, the strength of the latitudinal

temperature gradient is of sufficient size within this region that

geographic ranges with narrow latitudinal extents are still able to

capture a significant gradient. In contrast, the spatial distribution

of elevation temperature gradients reflects the form and extent of

orographic features and how species’ distributions intersect these

features. We found that the strength of these gradients varied

substantially across the globe and, unlike latitudinal temperature

gradients, differed significantly between threatened and non-

threatened species. In agreement with other studies [47,48],

species in Australia and the Islands of IndoMalaya stood out as

particularly vulnerable, with some of the shallowest elevational

gradients, followed by species located in the lowlands of the

Neotropics. In contrast to latitudinal gradients, our ability to

predict species’ elevational temperature gradients was limited,

reflecting the greater geographic heterogeneity in the location and

structure of these gradients.

The strength of both temperature gradients was positively

correlated with projected changes in temperature, but only for

species outside the tropics with latitudinal temperature gradients.

The greatest increases in temperature under climate change are

projected to occur at the high northern latitudes (see Figure S4).

Our findings therefore suggest a geographic correspondence with

the greatest projected warming occurring in regions with the

strongest latitudinal temperature gradients. However, few bird

species occur at the high northern latitudes year round. The

proportion of migratory species (ca. 19% of extant bird species

[49]) within breeding communities increasing linearly as you travel

north from the equator, approaching 100% at the highest latitudes

[50]. Migratory species spend the bulk of their annual cycle in

migration or on the non-breeding ranges at lower latitudes. Thus,

very few bird species are likely to benefit substantially from this

correspondence.

IUCN Red List categories of extinction risk are assigned using

the Red List criteria, which have quantitative thresholds relating to

population and range size, structure and trends [23]. Only 3.5% of

threatened or near threatened bird species (77/2193) are assessed

as threatened by climate change so severely that the global

population may be declining rapidly or very rapidly over three

generations, and hence potentially contributing to their Red List

category through the A criterion. Of these, only 26 (1.2%) actually

qualify under the A criterion. Our findings suggest this proportion

is likely to increase, especially for threatened species associated

with shallow elevational temperature gradients. As confirmed in

our analysis, threatened species occur primarily in the tropics and

their distributions are defined by smaller geographic ranges and

elevational extents. Hence, threatened species may be at a

geographic disadvantage under climate change with limited

associations with elevational or latitudinal temperature gradients,

although we found no evidence for the latter. Our findings suggest

Table 1. Coefficients and test statistics from robust linear models examining predictors of elevational temperaturegradients as estimated within the geographic ranges of 4,978 bird species.

Model Coef. SE t P

Intercept 3.149 0.380 8.29 ,0.001

Anomaly 0.976 0.108 9.05 ,0.001

Threat 23.117 0.895 23.48 ,0.001

Anomaly 6 Threat 0.344 0.273 1.26 0.2090

(R2 = 0.07)

Intercept 3.600 0.434 8.30 ,0.001

Size 0.511 0.074 6.92 ,0.001

Threat 21.872 1.076 21.74 0.082

Size 6 Threat 0.002 0.213 0.01 0.993

(R2 = 0.06)

Intercept 6.988 0.134 52.01 ,0.001

Shape 21.155 0.310 23.73 ,0.001

Threat 22.940 0.295 29.96 ,0.001

Shape 6 Threat 1.580 0.707 2.23 0.026

(R2 = 0.06)

Intercept 5.845 0.105 55.85 ,0.001

Orientation 0.018 0.002 8.18 ,0.001

Threat 21.824 0.280 26.52 ,0.001

Orientation 6 Threat 20.014 0.005 22.68 0.008

(R2 = 0.06)

Predictors include projected temperature Anomaly, geographic range Size, Shape, and Orientation and if the species is threatened with extinction (Threat).doi:10.1371/journal.pone.0098361.t001



threatened species that occur in the central tropics have higher

elevational evenness across their range, which is a likely

consequence of their distributions occurring on steep montane

slopes outside of lowland areas, which should result in stronger

elevational temperature gradients for these species. However, our

analysis suggests that the differences in elevational evenness

between threatened and non-threatened species was not substan-

tial enough to overcome the smaller elevational extents contained

within threatened species’ geographic ranges. Thus, our findings

suggest the weaker elevational temperature gradients identified for

threatened species is due in large part to a consistent association

with smaller elevational extents within their ranges.

When considering both gradients in combination, two regions

stand out as having both strong elevational and latitudinal

temperature gradients: western North America and Central Asia

(see Figures 3–4). These results suggest species in these regions will

have greater opportunities to track their climatic niches geograph-

ically. Depending on how these temperature gradients intersect

spatially within species’ ranges, some combination of these

gradients could be used. Similarly, two regions stand out as

having both shallow elevational and latitudinal temperature

gradients: the islands of IndoMalaya and the Amazon Basin in

South America (see Figures 3–4). Species in these regions are likely

to develop substantial range-shift gaps under climate change [10],

resulting in limited opportunities to track their climatic niche

geographically. Bird species occurring in the Amazon Basin are

also considered to have low adaptive capacity, which may increase

their vulnerability to climate change [51].

Species in tropical montane regions are more likely to have

restricted lateral and vertical distributions [48,52] and are also

more likely to be threatened with extinction (see Figure S3). Even

though in many cases these species occur in some of the most

Table 2. Coefficients and test statistics from robust linear models examining predictors of latitudinal temperaturegradients as estimated within the geographic ranges of 9,014 bird species.

Model Coef. SE t P

Intercept 20.288 0.021 213.61 ,0.001

Anomaly 20.092 0.006 216.52 ,0.001

Tropics 0.199 0.028 7.14 ,0.001

Threat 0.027 0.047 0.58 0.564

Tropics 6 Threat 0.028 0.019 1.48 0.138

Anomaly 6 Tropics 0.094 0.008 12.20 ,0.001

Anomaly 6 Threat 20.016 0.013 21.21 0.225

(R2 = 0.34)

Intercept 0.148 0.045 3.32 0.001

Size 20.120 0.007 217.09 ,0.001

Tropics 0.014 0.048 0.28 0.776

Threat 0.130 0.061 2.12 0.034

Tropics 6 Threat 20.034 0.020 21.66 0.098

Size 6 Tropics 0.080 0.008 10.38 ,0.001

Size 6 Threat 20.026 0.011 22.47 0.014

(R2 = 0.34)

Intercept 20.655 0.011 261.97 ,0.001

Shape 0.096 0.025 3.82 ,0.001

Tropics 0.591 0.012 47.91 ,0.001

Threat 20.005 0.335 20.02 0.988

Tropics 6 Threat 20.032 0.061 20.52 0.606

Shape 6 Tropics 20.134 0.028 24.70 ,0.001

Shape 6 Threat 0.129 1.018 0.13 0.900

(R2 = 0.35)

Intercept 20.687 0.006 2107.55 ,0.001

Orientation 0.002 0.000 13.52 ,0.001

Tropics 0.613 0.008 77.18 ,0.001

Threat 20.027 0.019 21.42 0.155

Tropics 6 Threat 20.026 0.019 21.34 0.180

Orientation 6 Tropics 20.002 0.000 212.49 ,0.001

Orientation 6 Threat 0.001 0.000 4.49 ,0.001

(R2 = 0.34)

Predictors included projected temperature Anomaly and geographic range Size, Shape, and Orientation and if the species is tropical (Tropics) or threatened withextinction (Threat).doi:10.1371/journal.pone.0098361.t002



extensive montane systems in the world, our findings suggest that

the overall steepness of elevational gradients is constrained by their

limited representation within species’ geographic ranges. Local

climatic heterogeneity, however, may allow for microclimatic

adjustments that could compensate for broader climatic trends

[53–56]. The level of climatic heterogeneity is determined by local

topographic variation and also by species’ habitat associations

[57]. For example, species in forested habitats may have greater

opportunities for microclimatic adjustments relative to species in

open habitats [58]. In general, however, behavior resulting in

microclimatic adjustments might not be sufficient to address the

full consequences of climate change [59].

Even if latitudinal and elevational temperature gradients are

readily available, dispersal along these gradients is not guaranteed.

Dispersal abilities are determined in large part by species’

morphological, physiological and behavioral characteristics and

adaptations [60,61], all of which are likely to be altered under

rapid climate change [62]. Dispersal under climate change may be

constrained by unsuitable habitat, population or habitat fragmen-

tation [58,63], or interspecific competition [64]. In addition, gene

flow that occurs in association with dispersal can both support and

hinder range-shift potential [65]. Gene flow among populations at

the leading edge of the range has been found to benefit fitness,

whereas gene flow from the interior to the leading edge has been

identified as maladaptive [66,67]. Dispersal abilities also vary

tremendously among species and between taxa [60]. Even highly

vagile taxa such as birds do not necessarily have the full

complement of behavioral or physiological characteristics needed

to support successful dispersal, which is considered particularly

relevant for tropical species [68,69]. Although there is evidence

tropical montane birds have moved upslope under climate change

[70], the low annual variation in temperatures within the tropics

relative to temperate regions may result in stronger physiological

barriers to dispersal for tropical species [52,71,72]. When tropical

habitats are fragmented through human activities – a process that

is occurring at an increasing rate – dispersal can become even

more constrained [73,74]. If species’ responses are hindered by

dispersal limitations or interspecific competition, as is expected for

many tropical montane bird communities, substantial ecological

disruptions are likely to occur [75].

In contrast, species that breed outside the tropics that are also

migratory [76] or have larger geographic ranges tend to have

stronger natal dispersal abilities [77–79]. Thus migratory species

that are broadly distributed and breed outside the tropics might be

in a better position to track elevational or latitudinal temperature

gradients. However, exceptions exist [80] and factors that are

strongly correlated with dispersal abilities might not be similarly

correlated with broad-scale distributional responses under climate

change [81]. Nevertheless, current evidence indicates distribution-

al responses for birds along latitudinal [7] and elevational

temperature gradients [82] are lagging behind warming trends,

suggesting stronger responses could develop as climate change

progresses and time lags are overcome [7].

We estimated temperature gradients in this study using

relatively high resolution environmental data that was finer than

the resolution of the species’ range data [30]. This grain mismatch

resulted in temperature gradients likely being estimated over fine-

grain sections of species’ ranges where probability of occurrence is

low. Our main results focus on the geographic form of the gradient

across the spatial breadth of species’ distributions, but future work

will benefit from further examination of potential biases this grain

mismatch may have on comparisons. How patterns of occurrence

are structured within species’ ranges, based on proportion of

occupancy and level of aggregation [83], may affect the chances of

successful dispersal along these gradients. For example, sparse or

fragmented patterns of occurrence may diminish the chances of

successful dispersal, while more continuous patterns of occurrence

may improve them. Alternatively, large contiguous regions with

low probabilities of occurrence might contain the steepest

gradients with very little dispersal value, as when lowland species’

distributions border mountain systems. These remaining uncer-

tainties highlight the need for advancing the spatial grain of our

global biodiversity knowledge and for the necessary collaborative

data mobilization, integration and quality control to realize this

[31].

In addition to temperature, other climate factors and conditions

are likely to be important in determining the strength and

importance of latitudinal and elevation temperature gradients in

defining range-shift potential. Two that have received particular

attention are changes in precipitation regimes and changes in

climatic variability. In contrast to temperature, precipitation has

more complex spatial and temporal variability and more complex

associations with latitudinal and elevational gradients. Projected

changes in precipitation are also more ambiguous [2], which adds

uncertainty to current estimates on how species are likely to

respond to climate change [84]. A second factor is climatic

variability, which is projected to increase through an increased

frequency of extreme climate events [2]. Temporal climatic

variability is considered an important factor defining species’

distributions limits [85] and increasing climatic variability can

have varied effects on species’ populations [86] including the

potential to hinder range shifts [87] and, especially under rapid

climate change, increase extinction risk [88].

Additional research is needed to improve our understanding of

how latitudinal and especially elevational temperature gradients

are structured within species’ ranges and the ability of species,

especially tropical, to take advantage of these gradients. In

particular, studies using higher resolution climate data (e.g., [22])

for species with varying spatial patterns of occurrence and forms of

elevational or latitudinal gradients would be informative. Birds are

often used as a model biological system due to high data

availability, but less vagile taxa also need to be considered such

as plants or vertebrate ectotherms that have alternative modes of

dispersal and different physiological and behavior capacities. With

birds, examining how these gradients are structured within non-

breeding ranges, where migratory birds tend to occur during the

majority of the annual cycle and are typically less well studied,

would be beneficial [9]. Efforts to better understand the role of

precipitation and climate variability in defining range-shift

potential along latitudinal and elevational temperature gradients

would support more comprehensive inferences.

Current efforts to project species’ distributions or to estimate

movement corridors under climate change often assume perfect

and complete dispersal along temperature gradients (e.g., [89]).

Temperature gradients are typically estimated using coarse-

grained interpolated weather-station data based on current

climatic conditions where the contrasting spatial forms of

latitudinal and especially elevational temperature gradients are

often poorly summarized [35,36]. These methods may exaggerate

estimated dispersal distances [90], especially at high northern

latitudes where latitudinal temperature gradients are projected to

weaken under climate change [12]. These considerations in

addition to the correlative nature of these models have promoted

the development of more mechanistic or process-based methods

intended to improve biological realism and minimize bias in

current projections [91]. Our findings suggest the quality of model

predictions may be improved by considering the spatial form and

strength of species’ demographic responses [92] to projected



latitudinal and elevational temperature gradients within species’

ranges and along possible movement corridors

Lastly, in order to maximize range-shift potential under climate

change, conservation efforts are needed to maximize the size of

areas of contiguous habitat, minimize the extent of habitat

fragmentation and promote the permeability of the matrix of

habitats around key sites. In particular, efforts to assess and

promote connectivity at broad geographic extents are likely to be

the most beneficial (e.g., [93,94]) where existing gradients are

represented as continuously as possible across space [95]. The

more thoroughly this can be achieved, the greater the potential for

species to track changing climatic conditions based on their unique

dispersal abilities and ecological and environmental requirements.

Conclusions

The availability of opportunities for geographic responses under

climate change reflects the interplay between each species’

geographic distribution and their associated latitudinal and

elevational temperature gradients (with the extent to which these

opportunities will be utilized depending on each species’ dispersal

abilities and the consequences of changing gene flow). The

distribution of these gradients across the world follows clearly

defined geographic patterns, but their availability depends on how

they intersect with species’ distributions. The location, size, and

shape of species’ geographic range and projected changes in

temperature all contain a degree of relevance in determining the

strength of these temperature gradients. However, the strength of

latitudinal and elevational temperature gradients varied consider-

ably among species, constraining our ability to make robust

predictions for all regions globally. Nevertheless, we found that

species that are currently at risk of extinction are consistently at the

greatest disadvantage, especially based on the availability of

elevational temperature gradients.

Supporting Information

Figure S1 Global patterns of elevation based on theUSGS global digital elevation model (GTOPO30) griddedat a 30 arc-second resolution (ca. 1 km at the equator).The solid grey line is the equator and the dashed grey lines are the

Tropics of Cancer and Capricorn (23.5uN and 23.5uS latitude,

respectively).

(PDF)

Figure S2 Global terrestrial annual mean temperaturefor 1950–2000 (WorldClim) averaged within 0.1 degreelatitudinal bands. The dotted lines indicate the Tropics of

Cancer and Capricorn (23.5uN and 23.5uS latitude, respectively).

(PDF)

Figure S3 Maps summarizing features of the globaldistribution of terrestrial avifauna across an equal areagrid (cell area: 3,091 km2). (A) The richness of all species

(n = 9,014) and (B) the richness of species threatened with

extinction (n = 878). (C) Geographic range size for all species

(n = 9,014) and (D) elevational extent for 4,978 species with

minimum and maximum elevation associations. (E) The evenness

of the distribution of elevation within each species’ range based on

the Gini coefficient and Lorenz curve (0 = high evenness; 1 = low

evenness) for 4,978 species with minimum and maximum

elevation associations. Maps are displayed using the Behrmann

equal-area cylindrical projection and the color ramps use Jenk’s

natural break classification. The solid grey line is the equator and

the dashed grey lines are the Tropics of Cancer and Capricorn

(23.5uN and 23.5uS latitude, respectively). Red lines distinguish

boundaries between six biogeographical realms.

(PDF)

Figure S4 Projected temperature anomalies summa-rized across species’ geographic ranges (map) andsummarized within six biogeographical realms (plots)as a function of the median latitude of each species’range. In the plots, red points are threatened species (n = 878) and

green points species non-threatened species (n = 8,136). Trend

lines are the fits of generalized additive models for threatened (red)

and non-threatened species (black). The solid line is the equator

and the dashed lines are the Tropics of Cancer and Capricorn

(23.5uN and 23.5uS latitude, respectively).

(PDF)

Figure S5 Fit of robust linear regression models to fourpredictors of elevational temperature gradients esti-mated within the geographic ranges of 4,978 birdspecies. Red points and lines are threatened species (n = 766)

and green points and black line are non-threatened species

(n = 4,212).

(PDF)

Figure S6 Fit of robust linear regression models to fourpredictors of latitudinal temperature gradients estimat-ed within the geographic ranges of 9,014 bird species.Green points and lines are for tropical species (n = 6,720), brown

points and lines are for extratropical species (n = 2,294). The solid

lines are the fits for non-threatened species (n = 4,214) and the

dashed lines are the fits for threatened species (n = 766).

(PDF)

Table S1 The 9,014 species considered in the analysis and their

estimated latitudinal and elevational temperature gradients,

designated biogeographical realm and threat status (1 = threat-

ened and 0 = non-threatened with extinction), projected temper-

ature anomaly, and geographic range size, shape and orientation.

(PDF)

Acknowledgments

We thank I. I. Mokhov for providing global lapse-rate values and three

anonymous reviewers for their constructive suggestions. We thank the large

number of experts and organizations who contribute information

incorporated into BirdLife International’s extinction risk assessments for

all species on the IUCN Red List, including spatial information

incorporated into the distribution maps.

Author Contributions

Conceived and designed the experiments: FALS KBG WJ. Analyzed the

data: FALS. Wrote the paper: FALS KBG WJ SHMB. Collected the data:

SHMB.

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Range-Wide Latitudinal and Elevational Temperature